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Domestication selected for deceleration of the circadian clock in cultivated tomato

Abstract

The circadian clock is a critical regulator of plant physiology and development, controlling key agricultural traits in crop plants1. In addition, natural variation in circadian rhythms is important for local adaptation2,3,4. However, quantitative modulation of circadian rhythms due to artificial selection has not yet been reported. Here we show that the circadian clock of cultivated tomato (Solanum lycopersicum) has slowed during domestication. Allelic variation of the tomato homolog of the Arabidopsis gene EID1 is responsible for a phase delay. Notably, the genomic region harboring EID1 shows signatures of a selective sweep. We find that the EID1 allele in cultivated tomatoes enhances plant performance specifically under long day photoperiods, suggesting that humans selected slower circadian rhythms to adapt the cultivated species to the long summer days it encountered as it was moved away from the equator.

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Figure 1: The circadian clock of cultivated tomato has been decelerated during domestication.
Figure 2: Two loci are responsible for variation in circadian rhythms between wild and cultivated tomato.
Figure 3: The EID1 region shows evidence of a selective sweep.
Figure 4: Differences in circadian phase affect overt phenotypes under diurnal conditions.

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Acknowledgements

We thank M. Koornneef and A. de Montaigu for helpful discussions and critical reading of the manuscript, U. Tartler and M. Pohe for technical assistance, members of the department, members of the Plan Breeding and Genetics Department at the Max Planck Institute for Plant Breeding Research and S.J. Davis for comments and advice, E.M. Willing for technical advice, and A.W. van Heusden for providing seeds and genotype information for the S. pimpinellifolium RIL population. We acknowledge funding from a core grant from the Max Planck Society. N.A.M., A.S. and C.L.W. were funded from a core grant from the Max Planck Society. M.R. was supported by funding from the German Research Foundation under the German-Israeli Project Cooperation program (DFG DIP project number FE552/12-1 awarded to J.M.J.-G.). D.Z. received a European Research Council Advanced grant (YIELD).

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Authors and Affiliations

Authors

Contributions

J.M.J.-G. and N.A.M. conceived and designed the research. J.M.J.-G., N.A.M., A.S. and M.R. performed and analyzed the RNA sequencing experiment. D.Z., N.R.S., J.N.M., I.O., A.R. and D.W. contributed the S. pennellii BIL population. S.H. and T.L. identified signatures of selection. C.L.W. isolated recombinant lines. N.A.M. performed all other experiments and analyzed the data. N.A.M. and J.M.J.-G. wrote the manuscript and all authors revised it.

Corresponding author

Correspondence to José M Jiménez-Gómez.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Circadian GI expression rhythms confirm differences found in circadian leaf movements.

(a) Mean relative GI (Solyc12g05660) expression ± SEM (n = 2) from qRT-PCR under constant light of two tomato species representative of cultivated tomato (red, S. lycopersicum cv. M82) and distant wild tomato (blue, S. pennellii LA0716); data are normalized against AP-2 complex subunit mu (Solyc08g006960); gray areas in the background indicate subjective nights. (b) Mean relative position of cotyledon tip of the same two species shown in (a); colored shading shows SEM (n = 36)

Supplementary Figure 2 Circadian LHY expression rhythms confirm differences found in circadian leaf movements.

(a) Mean relative LHY (Solyc10g005080) expression ± SEM (n = 2) from qRT-PCR under constant light of three tomato species representative of three tomato groups: cultivated tomato (red, S. lycopersicum cv. M82), ancestral wild tomato (orange, S. pimpinellifolium LA1589) and distant wild tomato (blue, S. pennellii LA0716); data are normalized against AP-2 complex subunit mu (Solyc08g006960); gray areas in the background indicate subjective nights. (b) For clarity, data from (a) are separated by species and scaled on the y-axis. The second half of the time-course for S. pimpinellifolium (middle panel) is vertically scaled 4:1 and the complete time-course for M82 (lower panel) 2.5:1.

Supplementary Figure 3 Cycling genes exhibit a substantially longer circadian period and later phase in cultivated tomato than in the wild relative S. pennellii.

(a) Circadian period and phase estimates of cycling genes (depicted by filled circles) in the tomato cultivar M82 (red, n = 731) and the distant wild relative S. pennellii (blue, n = 3001). The higher number of cycling genes in S. pennellii can be explained by the higher power to detect rhythms with an increasing number of cycles. Analysis of 1.3 cycles in S. pennellii (ZT12 to ZT40), i.e. the amount of cycles analyzed in the entire time-course for M82, identifies only 771 cycling genes. Translucent colors are used for visualization of the two-dimensional density. Circadian period and phase are both significantly different between species (Mann Whitney test, p < 2.2e-16). (b) Mean relative normalized expression of evening peaking genes; n = 38 for M82 (all genes with a phase between 10 and 11 and a period between 35 and 37) and n = 172 for S. pennellii (all genes with a phase between 10 and 11 and a period between 19 and 21). (c) Mean relative position of cotyledon tip (n = 36); gray areas in the background indicate subjective nights; Zeitgeber (ZT) time is defined as the time since the last dark-light transition. The longer period of the cycling transcriptome of cultivated tomato compared to leaf movements may in part be accounted for by the shorter time window and lower resolution. (d) Amplitudes of the genes shown in (a). The species exhibit a significant difference (Mann Whitney test, p < 2.2e-16).

Supplementary Figure 4 Expression patterns of tomato clock genes.

Mean normalized expression of clock gene homologs of S. lycopersicum cv. M82 in red and S. pennellii in blue; colored shading shows SEM (n = 2); the first 12 hours are sampled in the dark, indicated by a gray background in combination with a black bar in the x-axis. The following 60 hours represent constant light conditions; gray areas in the background in combination with a gray bar in the x-axis indicate subjective nights; Zeitgeber (ZT) time is defined as the time since the last dark-light transition. As in Arabidopsis, LHY/CCA1 and TOC1 seem to be reciprocally regulating each other. Another conserved feature is the sequential phasing of the pseudo-response-regulators (PRRs) over the day.

Supplementary Figure 5 Expression patterns of tomato clock genes.

Mean normalized expression of clock gene homologs of S. lycopersicum cv. M82 in red and S. pennellii in blue; colored shading shows SEM (n = 2); the first 12 hours are sampled in the dark, indicated by a gray background in combination with a black bar in the x-axis. The following 60 hours represent constant light conditions; gray areas in the background in combination with a gray bar in the x-axis indicate subjective nights; Zeitgeber (ZT) time is defined as the time since the last dark-light transition. As in Arabidopsis, the evening complex components ELF3, ELF4 and LUX peak around dusk.

Supplementary Figure 6 Expression patterns of tomato clock-output genes.

Mean normalized expression of clock output gene homologs of S. lycopersicum cv. M82 in red and S. pennellii in blue; colored shading shows SEM (n = 2); the first 12 hours are sampled in the dark, indicated by a gray background in combination with a black bar in the x-axis. The following 60 hours represent constant light conditions; gray areas in the background in combination with a gray bar in the x-axis indicate subjective nights; Zeitgeber (ZT) time is defined as the time since the last dark-light transition. Typical clock output genes in tomato show similar timing of expression as in Arabidopsis.

Supplementary Figure 7 The circadian clock of cultivated tomato changed in a stepwise manner.

Points in red and yellow represent mean circadian period and phase estimates ± SEM (n = 6-11) of seven ‘modern’ tomato cultivars and six accessions representative of the wild ancestor S. pimpinellifolium, respectively. These accessions serve as a reference and are marked with an asterisk in Supplementary Table 1. Each graph depicts in black mean circadian period and phase estimates ± SEM (n = 2-6) of tomato accessions representing sequential domestication steps. From more ancient to more modern: (a) Ecuadorian cherry tomatoes, (b) Mesoamerican cherry tomatoes and (c) Mesoamerican cultivars. Groups are framed by convex hulls of the according color for clarity. Each line was analyzed in at least two independent experiments.

Supplementary Figure 8 Circadian rhythm differences have a profound effect on the tomato transcriptome under diurnal conditions.

Phase distribution of the 2368 genes that cycle in both the cultivated tomato variety M82 (red) and the distant wild species S. pennellii LA0716 (blue). Samples were taken every four hours from plants grown under light dark cycles; phases were determined from an RNA-sequencing time course. Colored lines represent the kernel density estimation; black vertical lines indicate the two peaks of the kernel density.

Supplementary Figure 9 The phase QTL on chromosome 9 slightly lengthens the circadian period of cultivated tomato.

The QTL at the bottom of chromosome 9 is presented in an S. pimpinellifolium RIL population (a, b) and an S. pennellii IL/BIL population (c, d). (a) Logarithm of the odds (LOD) scores for circadian period. The dashed horizontal line indicates the 5 % significance threshold. (b) Mean period ± SEM of all RILs grouped by the maximally linked marker. (c) Genotypic representation of selected lines. S. lycopersicum = gray, S. pennellii = black. (d) Mean period estimates ± SEM of the lines shown in (c) (n = 10-22); colored shading indicates QTL genotype; each line was analyzed in at least two independent experiments.

Supplementary Figure 10 Confirmation and fine mapping of the phase QTL with two recombinant lines.

(a) Schematic genotype representation for the bottom of chromosome 9 of the recombinant lines (rec47 and rec38) and the lines crossed to generate them (M82 x IL9-2-6); S. lycopersicum = red, S. pennellii = blue; vertical lines outline the QTL; recombination breakpoints are indicated in Megabases (Mb). (b) Mean circadian phase estimates ± SEM (n = 10-12) of the lines shown in (a). Different letters indicate significant differences (one-way ANOVA and post-hoc Tukey’s HSD test, p < 0.05).

Supplementary Figure 11 Allelic variation of the coding sequence of EID1 underlies the phase QTL.

Mean relative position of cotyledon tip of T2 transgenic lines transformed with different promoter-cDNA combinations of EID1 or the empty vector (n = 54, 85, 82, 50 and 32 for M/M, p/M, p/p, M/p and empty, respectively). For each construct (except the empty vector) data from six to ten independent T2 populations are presented. The first letter of the legend labels signifies the promoter, the second letter the cDNA (M = S. lycopersicum cv. M82, p = S. pennellii); colored shading shows SEM; hatched areas in the background indicate subjective nights.

Supplementary Figure 12 Cultivated tomato is missing a lysine (K) in the highly conserved C terminus of EID1.

Alignment of the EID1 protein sequences of eight Solanaceae species: 1 = tomato (S. lycopersicum), 2 = ancestral wild tomato (S. pimpinellifolium), 3 = distant wild tomato (S. pennellii), 4 = potato (S. tuberosum), 5 = pepper (Capsicum annuum), 6 = eggplant (S. melongena), 7 = commercial tobacco (Nicotiana tabacum) and 8 = wild tobacco (N. benthamiana). Sequences were aligned using the ClustalW method; residues differing from the consensus sequence are marked by gray shading; colored bars on the top show the consensus strength indicative of the conservation level.

Supplementary Figure 13 Differences in circadian phase affect temporal gene expression waveforms under diurnal conditions.

Expression waveforms from qRT-PCR under long days and short days of three clock genes (TOC1, GI and LHY) and one clock output gene (CAB13) are compared between two recombinant lines only differing for the EID1 locus; the line carrying the wild species allele of EID1 (rec47) is shown in blue, the line with the cultivated allele (rec38) in red; data represent means of three biological replicates ± SEM; night samples, indicated by the hatched areas in the background, were taken in the dark. TOC1 levels keep rising in the darkness in rec38, whereas they immediately start falling in rec47, indicating that allelic variation at EID1 causes a slight phase shift also under diurnal conditions. However, for the morning-phased gene LHY no such shift is apparent. GI and CAB13 show a very clear increase of expression at the end of a long day in plants with the cultivated EID1 allele. Under short days, on the other hand, expression seems to be only slightly shifted.

Supplementary Figure 14 Phenotypic differences between the tomato cultivar Moneymaker and the wild ancestor S. pimpinellifolium under diurnal conditions.

The two accessions were grown under long days (18 hours light / 6 hours dark) and neutral days (12 hours light / 12 hours dark). (a) Mean height ± SEM (n = 8-9) four weeks after germination. (b) Mean days to flowering ± SEM (n = 8-9). (c) Mean relative chlorophyll content ± SEM (n = 8-9) measured with a SPAD chlorophyll meter four weeks after germination. Asterisks indicate significant differences (t-test, p < 0.05 *, p < 0.01 **, p < 0.001 ***). The much lower chlorophyll content of the wild species under long days, compared to Moneymaker, is due to incipient leaf chlorosis, potentially caused by circadian asynchrony due to the early phase and short period of the wild species. Although differences between cultivated tomato and the wild accession are visible also under short days, these are greatly reduced when compared to the differences under long days. In fact, the interaction between treatment and genotype in this experiment is highly significant in a 2-way ANOVA (p = 5.75e-06).

Supplementary Figure 15 Selection of period ranges for the analysis of the circadian RNA-seq time-course.

All analyses were conducted with the average of 2 biological replicates per time-point and species. (a) ARSER was run with the data of each of the species separately using an 8-hour wide sliding window starting from 4 and finishing at 44. The number of genes called as cycling by ARSER in each window (fdr_BH < 0.05) is shown as a heat map. (b) Histogram of the most significant period determined by ARSER for each cycling gene in each species. Based on this distribution we fixed the period ranges to be used for each species. These were 13 and 27 for S. pennellii and 22 and 42 for S. lycopersicum cv. M82.

Supplementary Figure 16 Phylogenetic trees of the 299 tomato accessions used for EID1 sequence analysis.

Neighbor-joining trees built with re-sequencing data from (a) ref. 28 and (b) ref. 27. Four thousand bi-allelic SNPs surrounding the chromosomal region of EID1 were used for each tree. Similar color in each tree represents the same species. Cultivated accessions that do not contain the putatively causal deletion in EID1, or wild accessions with the deletion, are marked with arrows for easy visualization.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–16, Supplementary Tables 3 and 5–9 and Supplementary Note (PDF 4243 kb)

Supplementary Table 1: Tomato accessions and their circadian variables.

List of tomato accessions evaluated for circadian rhythm analysis along with circadian phenotypes and their place of origin when available. (XLSX 51 kb)

Supplementary Table 2: Genotype information for the 15 BILs used for fine-mapping the phase and period QTLs.

Excel file with one sheet containing the physical coordinates for S. pennellii regions in the lines analyzed, and another sheet with their circadian parameters (XLSX 47 kb)

Supplementary Table 4: Tomato accessions used for the EID1 sequence analysis.

Accessions genotyped for the causative indel in EID1 along with the number of short reads showing presence / absence of the indel. (XLSX 60 kb)

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Müller, N., Wijnen, C., Srinivasan, A. et al. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nat Genet 48, 89–93 (2016). https://doi.org/10.1038/ng.3447

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